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Abstract

Background

Healthcare services often use a carbon monoxide (CO) breath test to validate self-reported
smoking and to assess reductions in smoking habit. A cut-off level of ≥ 8 parts per
million (p.p.m.) is used to identify smoking. This cut-off requires further validation
in pregnant women.

Methods

Data on self-reported smoking were assessed in conjunction with breath CO levels.
Subjects in the study were 2548 women attending antenatal booking during 12 months.

Results

546/2584 (21.4%) women self-reported as current smokers. A cut-off of 8 ppm identified
only 325/546 self-reported smokers (sensitivity 59.4%). 27/2002 self-reported non-smokers
had levels greater than 8 ppm (specificity 98.7%). Sensitivity and specificity analysis
revealed that CO cut-off levels of 2 or 3 p.p.m. resulted in the best sensitivity
and specificity for discriminating apparent smokers and non-smokers. A cut-off of
2 p.p.m. would have identified 468/546 of self-reported smokers (sensitivity 86%).
206/2002 self-reported non-smokers had levels > 2 ppm (specificity 90 %). If all these
women were 'true' smokers, the real prevalence of smoking in pregnancy was 26.5% (752/2548)
and 27% of true smokers provided false answers to the self-reported question at maternity
booking.

Conclusion

At 8 ppm, many smokers are missed and there may be gross underestimating of levels
of smoking in a pregnant population. Results emphasise the need to support a lower
cut-off level for the breath CO test closer to 2 or 3 p.p.m. These cut-offs may be
more appropriate in the antenatal clinic setting, and are in line with recent recommendations
in the non-pregnant population.

Background

Many studies have attempted to assess the effects of smoking during pregnancy on maternal
and child complications. Adverse consequences, including premature birth, low birth
weight and long-term sequelae including developmental problems such as cognitive delays
have been connected to maternal smoking [1,2].

A variety of factors have contributed to making it difficult to evaluate the effects
of smoking during pregnancy. These include errors in measurement such as maternal
denial and under-reporting, fluctuating behaviour of smoking during pregnancy and
metabolism, including accelerated metabolism during pregnancy [3].

It is important clinically to have knowledge of patients smoking habits since it enables
appropriate anti-smoking advice to be given and pregnancy is seen as a window of opportunity
to provide this. Meta-analyses, including a Cochrane review, show that appropriate
screening plus active intervention, in the form of advice and provision of written
materials, increases the numbers of pregnant women who stop smoking. This in turn
can reverse the adverse effects of smoking on perinatal outcomes by up to 20% [4,5]. It has also been emphasised that, in pregnancy, biochemical validation can increase
women's motivation to stop smoking and increase their utilization of available treatment
services [6], though a recent review showed no evidence that biofeedback motivated cessation [7].

In the general population, the proportion of people who report to be non-smokers but
show biochemical levels indicative of smoking are generally low [8]. In pregnancy, however, women who smoke can experience intense social and clinical
pressure that results in false declarations of non-smoking. This inaccuracy of self-reported
smoking makes appropriate counselling difficult and stresses the need for reliable
biochemical confirmation of smoking status [9].

Of the biochemical measures to assess smoking, cotinine, a metabolite of nicotine
found in the blood and urine, is most preferred by scientists because of its long
half-life, averaging 17 hr in non-pregnant women [10] and 9 hr in pregnant women [11]. In the clinical setting however, breath carbon monoxide (CO) level is seen to provide
an immediate, non-invasive method of assessing smoking status and is the method most
suitable to the antenatal clinic [12]. It is less preferred as a biochemical marker because CO has a short half-life of
approximately 1–4 hours [13] and may not detect low levels of smoking [14]. Furthermore, the development of relatively inexpensive portable CO monitors enables
breath CO levels to be assessed in a wide variety of clinical settings [15].

Currently in Glasgow, all women attending the antenatal clinic are CO monitored and
those with a reading of ≥ 8 ppm or self-reported smokers are directly referred to
a smoking cessation link midwife for a 6 week support programme. Since the results
of the CO test and or self-report are the critical factors for referral for cessation
advice, the accuracy of these is paramount to providing intervention. The 8 ppm cut-off
in this programme is based on a standard cut-off for abstinence verification that
is widely accepted within the research community [16]. New evidence suggests that this may not be appropriate in all settings. Recently,
Javors et al concluded that the cut-off should be lowered to 2 or 3 ppm for assessment
of smoking in a general population and a cut-off of 4 ppm in post partum women was
suggested [17,18].

The present study examines the sensitivity and specificity of the breath CO test,
and the optimal cut-off level to distinguish smokers from non-smokers amongst pregnant
women.

Methods

Data was collected at the antenatal booking appointment when women have a form completed
by a nursing auxiliary along with the results of a CO breath test. These forms were
obtained from the office for the Scottish smoking intervention programme called 'Breathe',
in the Southern General Maternity Unit, Glasgow. Ethical approval was obtained from
the Local Research Ethics Committee.

The Southern General Hospital has an 85–90% rate of return for the Breathe service
forms of all women booked; the results of the present report are therefore likely
to be applicable to the general pregnant population. Women who provided relevant Breathe
forms and booked for antenatal care in the Southern General Hospital Glasgow between
the months of July 2005 and June 2006 were included in this study.

The cut-off level for a CO test indicates that a result at or above (≥) the cut-off
level would be a positive test for a smoking day (presumed to have smoked). A CO level
below the cut-off would be a negative test (presumed a non smoker). In this study,
various CO cut-off levels were used to evaluate cut-off levels for their accuracy
in identifying pregnant smokers and non smokers. For example, CO level of 3 p.p.m.
would be a positive test at a CO cut-off of 3 p.p.m.

Study Procedure

All Breathe forms for women who booked between the months of July 2005 and June 2006
were inspected. Data on these forms is recorded by a midwife or auxiliary nurse at
the antenatal booking clinic. At the clinic, the CO test is offered at a point suited
to the midwife/auxiliary nurse and the test itself is performed using the EC50 Smokerlyzer
(Bedfont Instruments; Kent, UK), an inexpensive, portable CO monitor that has previously
been shown to be effective [15]. Midwives and auxiliary nurses have a two hour accredited training session regarding
use of the device.

Data extracted from the forms included: self-reported smoking status, CO levels measured
at the booking visit, date of birth, date of booking, number of cigarettes smoked
per day and any additional comments made by the women.

Statistical methods

Self-reported smoking and CO validated smoking status were analysed descriptively,
using sensitivity and specificity percentages. Sensitivity was defined as the percentage
of positive CO tests (a CO level at or above a given cut-off) for self-reported smokers,
i.e. the percentage of all self-reported smokers for which there was a positive CO
test. Specificity was defined as the percentage of negative CO tests (a CO level below
a given cut-off) for self-reported non-smokers, i.e. percentage of all non-smokers
for which there was a negative CO test. (Sensitivity + specificity) divided by 2 was
calculated for each possible cut-off to identify the CO cut-off level that would have
the highest average of combined sensitivity plus specificity.

Data were analysed by the SPSS 14 and Minitab 14 statistical packages.

Results

Levels of smoking, and sensitivity, specificity of self-report against carbon monoxide
(CO)

Of the 2661 women in the 'Breathe' dataset 2650 (99.6%) had self reported smoking
data and 2548 (95.8%) had both self reported smoking data and CO validated measurements.
Of these 2548 women, n = 2002 (78.6%) reported they were non-smokers and n = 546 (21.4%)
were current smokers. 13.9% (n = 354) of women had a CO level of = 8 p.p.m. and were
categorised by the current cut-off as validated smokers. The CO breath test results
and self reported smoking status for all subjects are shown (Table 1, Figure 1).

Figure 1.Bar Chart of CO measurements for non-smokers and smokers. The four lines indicate a) and b) 2 and 3 p.p.m.: the cut-off points with highest
sensitivity and specificity c) 5 ppm: the new cut off for the Breathe programme and
d) 8 ppm: the current cut-off point. It is possible to visualise the increase in number
of subjects picked up by the test as the cut-off point is lowered. Note: The scale
for the frequency of women has been truncated so as to remove the large peak of non-smokers
at 1 p.p.m. (n = 1790). This allows the results for all women to be visualized more
appropriately.

Alternative Carbon Monoxide cut-off levels

As the CO cut-off increased in value from 1 to 12 p.p.m., sensitivity decreased and
specificity increased (Table 2). The highest average for combined sensitivity and specificity (88%) was observed
at a CO cut-off level of 2 and 3 p.p.m. When plotted (Figure 2), the sensitivity and specificity curves intersect at a CO level between 2 and 3
p.p.m. This intersection indicates that the highest combined sensitivity and specificity
was observed at a CO cut-off level less than 3 p.p.m.

Relationship between cigarettes smoked per day and CO levels

The mean CO levels increase with increasing number of reported cigarettes smoked (Figure
3). The maximum and minimum CO values illustrate the overlap for CO levels between
the categories for numbers of cigarettes smoked.

Figure 3.Mean CO levels for each cigarette category with 95% confidence intervals for all reported
smokers (N = 546). The mean CO value for all smokers in each category is shown above the bar. The minimum
and maximum CO levels for those smoking <10, 11–20, 21–30 and 30+ cigarettes are,
1–34, 1–35, 4–37 and 13–36 p.p.m. respectively.

Discussion

The current paper examines the relationship between self-reported smoking status and
validated smoking status using the Carbon Monoxide (CO) breath test. Results show
that, with a sensitivity of 60%, the cut-off level of 8 ppm used for CO tests in the
antenatal booking clinic is insufficiently sensitive. Of the 546 women who reported
to be smokers 219 had CO values <8 ppm. Other than the possibility of data input error
by midwives and nurses, there i, s no reason to presume women would say they smoke
when they do not. It seems likely, therefore, that their smoking levels were too low
to be detected and that the cut-off point for the CO test to improve detection of
smokers requires adjusting downwards. This is especially important as light smokers
are more likely to respond to smoking cessation intervention. It is important to recognise
that breath CO has a short half-life of approximately 1–4 hours and thus it may not
detect low levels of smoking [14]. In this study, the lower level of cigarette smoking in women who did not reach a
cut-off of 8 ppm reflects this.

Evaluation of alternative cut-off levels pointed to a CO cut-off of 2 or 3 p.p.m.
providing the highest accuracy for assessment of abstinence of smoking in this population.
This cut-off was confirmed by several analyses. When the cut-off level was lowered,
the sensitivity and specificity for self-reported smoking against CO, at 86% and 90%
for 2 p.p.m. and 83% and 93% for 3 p.p.m., respectively, were high. This contrasts
to the lower average of combined sensitivity and specificity observed at a cut-off
of 8 ppm. Javors et al [17] recently suggested that a cut-off of 2 to 3 p.p.m. is more appropriate for detecting
smokers within the general population. The current paper concurs with cut-off levels
of 2 ppm and 3 ppm in the antenatal clinic setting to detect, with reasonable accuracy
and discrimination, women who are smokers.

Accuracy of self reported smoking

There is a caveat with regard to the use of self reported smoking to establish the
CO cut-off. In Scotland the proportion of pregnant women smoking at booking is approximately
25% and in Glasgow this figure is even higher at 31.2% [19]. The proportion of self reported smokers in the current study population was 21%
indicating that at least 10% of women in this population are potentially not telling
the truth about their smoking status. This inaccuracy in reporting could explain why
many reported non-smokers had CO levels beyond 2–3 p.p.m. and why 27 reported non-smokers
had readings ≥ 8 p.p.m. There were some interesting comments made by women who reported
as non-smokers but who had high CO levels:

• "..sitting in front of a smoker on the bus here" (24 ppm)

• "Gas fire needs fixing" (13 ppm)

• "Walked under the bridge on the way here – a lot of pollution" (9 ppm)

There are suggestions that changes in pregnancy may increase CO absorption from non-smoking
sources, particularly later in pregnancy [20]. However, the contribution of environmental smoke exposure is multifactorial and
difficult to assess: the reported cause is unlikely to be a sound measure of exposure.
At such high levels one can almost be certain these women are denying their smoking
status and that reporting exposure to environmental sources may have offered a "way
out" for some women who did not want to admit to smoking. The Information Services
Division for Scotland (ISD) states that the data on smoking behaviour are: "...based
on self-reported information obtained from mothers at their ante-natal booking visit
in the community or at hospital." The lower prevalence of smoking found in this study
population may indicate that self reported smoking is not accurate in the antenatal
clinic setting. Since the ISD use self reported smoking at the antenatal booking clinic
to quantify the number of pregnant smokers, they are potentially under-estimating
levels of smoking in the Scottish population. Thus, self reported smoking is an imperfect
method of recording smoking status in this population.

CO p.p.m. versus self reported intensity of smoking levels

There is considerable overlap in CO levels for all categories of number of cigarettes
smoked. For example, a woman smoking 21–30 cigarettes could have the same reading,
as low as 4 ppm, as a woman smoking 10 or fewer cigarettes. Time since last cigarette
and CO testing and also underreporting of number of cigarettes smoked requires further
study with direct measures such as cotinine to support findings in this study that
the CO test is poor at distinguishing between different intensities of cigarette smoking.
Since the CO means are noticeably different for the various smoking categories the
CO test may be useful for showing only major changes in reduction of cigarette intake,
and this could be used as a motivational tool.

It is recognised in current literature that light smokers (women smoking less than
10 cigarettes per day) are significantly more likely to quit during pregnancy [21]. It is therefore essential that any screening programme identifying smokers must
pick up with accuracy, this population of pregnant smokers.

Policy Issues

It has been documented in studies in New Zealand and the US that at maternity booking
or at the end of pregnancy, over 20% of pregnant smokers falsely categorise themselves
as non-smokers when asked by their midwife. This is the method used in the UK to identify
pregnant smokers in order to refer them for specialist smoking cessation support.
[22]

The under-reporting is likely to result from fear of disapproval rather than because
these women don't want to stop smoking. There is a recognised policy in the UK to
establish services for pregnant smokers. If the identification system (self-report
at maternity booking) misses out 20% of pregnant smokers, by not recognising them,
they are denied an important service. It is therefore important to identify their
smoking habit in a less judgmental fashion: perhaps in the same way that all women
in the UK are screened at maternity booking for syphilis by testing their blood samples.
Our study shows that CO breath testing at the recognised cut-off does not accurately
detect smokers, particularly low level pregnant smokers who are a target group. Another
biochemical marker such as cotinine in blood or urine may be required to identify
all pregnant smokers so they can benefit from specialist smoking cessation support
and to assess the effectiveness of interventions. The role of clinicians is not necessarily
to ensure the success of making all smokers quit, but rather to provide a reliable
cessation service that is offered to all those who smoke. Increasingly, smoking cessation
services are using the CO breath test for verification of non-smoking. The Breathe
Tobacco Planning Interest Group state that the importance of the CO test is in its
ability to demonstrate an immediate and potentially harmful consequence of smoking,
and, consequently, to increase the number who take part in the programme and comply
with advice to quit. By missing a large proportion of smokers, the test does not achieve
this effectively. As a consequence of the current research the Planning Group have
changed policy in antenatal clinics and reduced the CO cut off point to ≥ 5 ppm. This
cut-off was seen as most appropriate when balanced with available resources and in
future may be reduced further.

Limitations

It was not possible to control for the issue of time since last cigarette and as a
result it is possible that a woman who smokes prior to the clinic will have a very
different CO reading to a woman who smokes after the clinic. It is also possible that
women who self reported as non-smokers may have been light smokers, and may not have
exceeded a CO level of 2 or 3 ppm; thereby reducing further the correlation between
self report and biochemical measures. Lower CO levels observed during pregnancy do
not necessarily reflect less smoke exposure, and cut-off levels used to classify non-smokers,
passive smokers, and active smokers need to be established for pregnancy. It can be
expected that the quality of measurement performed by midwives is variable. A further
limitation was the use of participant self-report as the "gold standard" to determine
smoking status. Cotinine or thiocyanate are possible alternative biomarkers of smoking
for future study.

Conclusion

At a cut-off of 3 ppm 113 (4.4%) more women would have been offered smoking cessation
advice. The consequences of referring non-smokers depend on the number wrongly being
referred. At 3 ppm a total of 113 of self-reported "non-smokers" will be contacted.
Midwives in the service state that this is not a problem as most women will state
this when contacted and no further contact will be made by the midwife. The impact
on finances and resources is an issue. To accurately assess this it would be necessary
to consider the number of women wrongly being referred versus the long term benefits
of contacting a denier who then proceeds to use the service and quit. The costs of
contacting all women, "a blanket referral", would most certainly outweigh the costs
of carrying out a CO test and therefore an appropriate cut-off is important to maximise
cost-benefit outcomes.

At 8 p.p.m., many smokers are missed and there may be gross underestimating of levels
of smoking in a pregnant population. Results emphasise the need for further research
to support a lower cut-off level for the breath CO test closer to 2 or 3 p.p.m. This
may be more appropriate in the antenatal clinic setting, and is in line with recent
recommendation in the non-pregnant population.

Authors' contributions

ZCU carried out the research, and wrote the manuscript. PC participated in the supervision
and coordination of the project. DS performed the statistical analysis. DT participated
in the design and coordination of the study and helped to draft the manuscript. All
authors read and approved the final manuscript.

Acknowledgements

The researcher is grateful to Professor Sattar for his support, midwives D Barnett
and M Nsofor for their help, B Whyte, and H Gilmour for contributions to statistical
analysis. This study was supported and funded by Glasgow University and Glasgow Centre
for Population Health.

References

Sattar N: Do pregnancy complications and CVD share common antecedents?